Differential modulation of spontaneous and evoked neurotransmitter release from hair cells: Some novel hypotheses

Guth, Paul S.; Aubert, Anne; Ricci, Anthony J.; Norris, Charles H.

doi:10.1016/0378-5955(91)90155-3

Cited by 46 publications

(10 citation statements)

References 33 publications

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“…Our findings are consistent with the expression of AMPA reccptors in cultured neurons in accordance with the proposed glutamatergic neurotransmission at the synapses between sensory hair cells and the afferences of the primary vestibular neurons zn vivo (Annoni et al, 1984;Bledsoe et al, 1988;Guth et al, 1988Guth et al, , 1991Soto and Vega, 1988) and the suggestion that the excitatory signal from sensory cells is mediated predominantly by non-NMDA glutamate receptors (Prigioni et al, 1994). This correspondence validates this model system for extensive analysis of the expression of the different GluRs in the vestibular ganglion neurons.…”

Section: Calcium Variations In Cultured Vestibular Ganglion Neuronssupporting

confidence: 91%

AMPA Receptors in Cultured Vestibular Ganglion Neurons: Detection and Activation

Rabejac

Devau

Raymond

1997

Eur J of Neuroscience

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The presence and the activity of alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid (AMPA) glutamate receptors were investigated in mouse cultured vestibular ganglion neurons using immunocytochemistry and measurement of intracellular calcium concentration ([Ca2+]i) by spectrofluorimetry. Cultures of dissociated vestibular ganglia from 18 gestation day mouse embryos were grown in vitro for 3-4 days. Immunocytochemical labelling of AMPA receptor subunits GluR2/R3 and GluR4 was detected in neuron cell bodies and proximal neurites and more lightly in glial cells. There was no clear selective subcellular localization of the different subunits. For the GluR1 subunit a signal was observed only in some neurons and neurites and was weak. Vestibular ganglion neurons responded to fast application of 1 mM glutamate and 10 mM aspartate through unknown receptors by a transient increase in [Ca2+]i. The mean amplitude of this rapid increase was about nine times the resting level and recovery was complete within 30-45 s after the application. If separated by an interval of at least 10 min, consecutive applications produced similar calcium responses. AMPA (1 mM) application induced the same type of responses. Five minutes prior to the AMPA exposure, the application of a specific AMPA antagonist, 6,7-dinitroquinoxaline-2,3-dione (DNQX, 1.5 mM), in the external medium inhibited the response to AMPA. Chelation of external calcium by EGTA (1.5 mM) abolished the responses to drug applications, indicating that an influx of external calcium is involved in the [Ca2+]i increase. These observations suggest that heteromeric AMPA receptors are expressed in vestibular ganglion neurons in culture and play a functional role in their glutamate-induced depolarization. Experiments are in progress using specific AMPA and NMDA antagonists to characterize the participation of the two types of ionotropic glutamate receptors in the glutamate/aspartate-induced intracellular calcium response.

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Section: Calcium Variations In Cultured Vestibular Ganglion Neuronssupporting

confidence: 91%

AMPA Receptors in Cultured Vestibular Ganglion Neurons: Detection and Activation

Rabejac

Devau

Raymond

1997

Eur J of Neuroscience

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“…However, extracellular recordings from canal afferents in the turtle indicate that NMDA, like glutamate and aspartate, has a potent excitatory effect (Cochran and Correia, 1995), which would suggest a direct receptor role for NMDA. The hair cell autoreceptor (Soto and Vega, 1988;Prigioni et al, 1990;Devau et al, 1993), instead, may utilize AMPA receptor subtypes (GluR1 and GluR2/3; Dememes et al, 1995) and/or group I metabotropic receptors (Guth et al, 1991;Hendricson and Guth, 2002).…”

Section: Discussionmentioning

confidence: 99%

γ‐Aminobutyric acid is present in a spatially discrete subpopulation of hair cells in the crista ampullaris of the toadfish Opsanus tau

Martinelli

Henderson

Friedrich

et al. 2004

J of Comparative Neurology

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Although gamma-aminobutyric acid (GABA) and glutamate are known to be present in the vestibular sensory epithelia of a variety of species, the functional relationship between these two transmitters is not clear. The present study addresses the three-dimensional spatial distribution of GABA and glutamate immunoreactivity in the vestibular labyrinth of the oyster toadfish by using whole end organs labeled by immunofluorescence with monoclonal anti-GABA and/or antiglutamate antibodies and visualized as whole mounts by multiphoton confocal microscopy. We find glutamate-immunoreactive hair cells present throughout the sensory epithelium. In contrast, prominent GABA immunoreactivity is restricted to a small population of hair cells located in the central region of the crista. Double immunofluorescence reveals two distinct staining patterns in GABA-labeled hair cells. Most ( approximately 80%) GABA-labeled cells show trace levels of glutamate, appropriate for the metabolic/synthetic role of cytoplasmic glutamate. The remainder of the GABA-stained cells contain substantial levels of both GABA and glutamate, suggesting transmitter colocalization. In the toadfish utricle, glutamatergic hair cells are present throughout the macula. GABA-immunoreactive hair cells follow the arc of the striola, and most GABA-labeled receptor cells coexpress glutamate. The localization of GABA was explored in other species as well. In the pigeon, GABAergic hair cells are present throughout the crista ampullaris. Our findings demonstrate that multiple, neurochemically distinct types of hair cells are present in vestibular sensory epithelia. These observations, together with the excitatory activity generally associated with 8th nerve afferent fibers, strongly suggest that GABA serves an important, specific, and complex role in determining primary afferent response dynamics.

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“…In fact, it may be argued that steady state firing requires recruitment of vesicles such that the rate of release at any given synapse may be dictated by access to the reserve pool of vesicles. Thus it may be that spontaneous firing rates are regulated by resting calcium currents and vesicles in the RRP and recycling pool, while stimulated release is more dependent upon vesicle recruitment form the reserve pool and the ability to module release of stored calcium (Guth et al, 1991). …”

Section: Discussionmentioning

confidence: 99%

Calcium-Dependent Synaptic Vesicle Trafficking Underlies Indefatigable Release at the Hair Cell Afferent Fiber Synapse

Schnee

Santos‐Sacchi

Castellano-Muñoz

et al. 2011

Neuron

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Sensory hair cell ribbon synapses respond to graded stimulation in a linear, indefatigable manner, requiring that vesicle trafficking to synapses is rapid and non rate limiting. Real time monitoring of vesicle fusion identified two release components. The first was saturable with both release rate and magnitude varying linearly with Ca2+, however the magnitude was too small to account for sustained afferent firing rates. A second superlinear release component required recruitment, in a Ca2+-dependent manner, of vesicles not in the immediate vicinity of the synapse. The superlinear component had a constant rate with its onset varying with Ca2+ load. High-speed Ca2+ imaging revealed a nonlinear increase in internal Ca2+ correlating with the superlinear capacitance change, implicating release of stored Ca2+ in driving vesicle recruitment. These data, supported by a mass action model, suggest sustained release at hair cell afferent fiber synapse is dictated by Ca2+-dependent vesicle recruitment from a reserve pool.

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Differential modulation of spontaneous and evoked neurotransmitter release from hair cells: Some novel hypotheses

Cited by 46 publications

References 33 publications

AMPA Receptors in Cultured Vestibular Ganglion Neurons: Detection and Activation

AMPA Receptors in Cultured Vestibular Ganglion Neurons: Detection and Activation

γ‐Aminobutyric acid is present in a spatially discrete subpopulation of hair cells in the crista ampullaris of the toadfish Opsanus tau

Calcium-Dependent Synaptic Vesicle Trafficking Underlies Indefatigable Release at the Hair Cell Afferent Fiber Synapse

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